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Orangutan mating behavior and strategies

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DOI: 10.1093/acprof:oso/9780199213276.003.0016

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 CHAPTER 16

Orangutan mating behavior

and strategies
S. Suci Utami Atmoko, Tatang Mitra Setia, Benoit Goossens,
Sheena S. James, Cheryl D. Knott, Helen C. Morrogh·Bernard,
Carel P. van Schaik and Maria A. van Noordwijk

Photo C Herman D. Rijk.sen

least one sex find the other. The mating system of

16.1 Introduction orangutans is of interest because it is based on an
In species where both sexes are more or less soli- interaction between female choke and male har-
tary, such as orangutans, mating requires that at assment and coercion, against a background of

235
236 ORANGUTANS

intense male-male competition, which has pro- male-male competition predominate (Schlirmann
duced extreme sexual dimorphism and is accom- and van Hooft, 1986; Rodman and Mitani, 1987).
panied by very unusual male bimaturism. Behveen-male contest competition must clearly
The aim of this chapter is to assess how these have contributed to the development of the extreme
three aspects of sexual selection (male competi- sexual dimorphism of this species. Indeed, Rodman
tion, female choice and mating conflict) interact to and Mitani (1987) proposed it as the sale factor.
produce the mating behavior of orangutans. After However, because fema les selectively approach
a theoretical introduction and a review of what is or allow themselves to be approached by flanged
known about orangutan mating behavior, we pre- males when they are in their fertile periods, 'female
sent a compilation of basic data from various sites choice' must also playa critical role in maintaining
in order to assess whether the broad picture built male physical characteristics.
up over the years is similar throughout the orang- Another unusual feature of the mating system
utan's geogrnphic range. of orangutans is the occurrence of forced mat-
Orangutans have a semi-solitary life style. ings ('rapes') (Rijksen 1978; Galdikas 1979, 1985b, c;
Individuals usually live alone in highly overlap- Mitani 1985a, b; Fox 1998, 2002). Even though pre-
ping home ranges, and at some sites they occasion- mating aggression and physical coercion to mate
ally aggregate in large fruit trees or groves (see are seen in other primates, orangutan females seem
Chapter 17). During times of high fruit abundance, to resist mating attempts by particular males much
these aggregations develop into travel bands, in more strongly than seen in other species. Mating
which individuals travel together in a coordinated resistance, in which a fema le struggles and attempts
fashion (Sugardjito et al. 1987; Utami et al. 1997; to prevent intromission while the male attempts to
van Schaik 1999; Singleton and van Schaik 2002). restrain the female by grabbing and holding on
Consortships, a form of travel band in which a to her arms, legs and body, can result in a fierce
malc-female pair may range together in a coordi- physical fight between a male and a female (and
nated way for several days, weeks or even months sometimes her YOWlgest offspring). These inter-
and engage in sexual behavior, are seen at all sites. actions may involve hitting, pushing and biting by
Other individuals (females, unflanged males and all involved and whimpering, squealing, grumph-
adolescent individuals) may also associate around ing, kiss-squeaking and other vocalizations by the
a consort pair (Schurmann and van Hooff 1986), female and/or her offspring. The level and timing of
although fully mature, flanged males never asso- female cooperation and resistance is variable: some
ciate together and usually behave antagonistically male mating attempts may start with resistance and
toward each other (see Chapter 15). continue passively or even cooperatively, others
Orangutans have three striking features for pri- may start cooperatively but end with resistance
mates: (1) extreme sexual dimorphism in body size, (Fox 1998), making classification complicated. Since
(2) forced matings, and (3) bimaturism among males. females resist mating attempts by particular males
As in many other dimorphic primate species, the sex- even when no other males are present (and may
ual dimorphism in body size arises because males not even be within hearing distance) this behavior
continue to grow beyond the age at which females is unlikely to incite direct male-male competition
stop growing. In orangutans, male growth continues as suggested for other species with conspicuous
gradually until well after the twentieth year of age female mating resistance (e.g. Cox and LeBoeuf
(,indeterminate growth', Leigh and Shea [1995]). In 1977; Boness et 01. 1982) but seems to be an honest
addition to larger body size, the male secondary sex- reflection of female preference (Fox 1998, 2002). So
ual characters (SSCs) consist of flanged cheeks and a far, in all populations females have been observed
throat sack, with which they can produce long calls to engage in a wide range of mating interactions
to advertise their presence (MacKinnon 1974; Rijksen from female-initiated active participation to fiercely
1978; Rodman 1984; Galdikas 1985b). contested, with many variations in between.
Hypotheses to explain sexual dimorphism Perhaps the most unusual feature of orangutans
invoke sexual selection in which female choice or is the remarkable individual variation in the age
 ORANGUTA N MATI NG BEHAVIOR AND STRATEG IE S 237

at which sexually mature males develop their This chapter considers the mating strategies of
SSCs-a phenomenon called bimaturism (Uchida males and females and their interactions, based on
1996; Maggioncalda et al. 1999, 2002). In some field studies in Ketambe (Sumatra), Suaq Balimbing
males, at least in Sumatra, this development may (Sumatra), Gunung Palung (West Kalimantan),
be delayed until the male is well over 30 years old Tanjung Puting (Central Kalimantan), Sabangau
(Utami Atmoko 2000; Utami et al. 2002), some 20 (Central Kalimantan), Tuanan (Central Kalima ntan),
years after reaching sexual maturity and at least Kutai (East Kalimantan) and Kinabatangan (Sabah).
15 years after reaching the size of adult females. Table 16.1 gives an overview of the database used
Although these unflanged or 'arrested' males lack for this chapter.
SSCs, they are fertile, sexually active and able
to sire offspring (Kingsley 1982; Maggioncalda
et al. 1999, 2002; Utami Atrnoko 2000; Utami, et al. 16.2 Mating behavior of orangutans
2002). This bimaturism leads to the coexistence of
16.2.1 Ontogeny of mating behavior
two adult, sexually mature morphs: flanged and
unflanged males. Mating behavior is not unique to adult and ado~
The presence of an uncontested flanged male lescent individuals. In Ketambe, infants as young
has been proposed as a key proximate factor main- as two years of age, of either sex, already show
taining developmental arrest in unflanged males, keen in terest in sexual behavior. For instance, the
at least in captivity (Kingsley 1982; Graham and infant male Yossa sometimes masturbated as part
Nadler 1990; Maggioncalda et al. 1999, 2002; Utami of his play behavior, sometimes using his own
Atmoko 2000). However, this is unlikely to work hands or feet, once using a stick, and occasion·
in the wild, where the two kinds of males inhabit ally even thrusting into his mother's vagina while
large ranges widely overlapping with those of she was h anging. Immatures also directed sexual
many others, flanged and unflanged. Utami et al. beh avior at each other, especially when they were
(2002) could show that two early hypotheses for playing. For instance, 6-year-old female Tati had
the evolution of bimaturism were inconsistent 3-year-old Yassa masturbate her, and afte r that she
with the data. The data reviewed in this chap- masturbated him. During rest, orangutan mothers
ter can be used to evaluate other hypotheses (see often licked their infant's genitals to clean them,
discussion). and this may be the first sexual experience for

Table 16.1 Overview of the database llSed for this chapter

Site Period Researchers

Sumatra
Ketamhe 1972-1978 H.D. Rijksen, c.l. Schfirmann
1979-1996 Ketamhe orangutan project Universitas Nasional
Jakarta- Utrecht University Netherlands
Suaq Balimbing 1994-1999 Suaq !lalimbing orangutan project Universitas
Indonesia Jakarta-Duke University USA
Borneo
Kinabatangan 2000-2003 M. Ancrenaz, s.s. James
Kutai NP 1981-1982 J. Milani (1985b)
Sabangau 2003- 2005 H. Morrogh-Bernard
Tuanan 2003-2006 Tuanan orangutan project Universitas Nasional
Jakarta-University of Zurich, Switzerland
Tanjung PUling 1971-1975 B.MJ. Galdikas (1979, 1981, 1985a, b)
Gunung Palung 1994- 2003 CD. Knott

'See the Preface and Chapter 7 for descriptions of habitat.

238 ORA NGUTA NS

young individuals. They also acquire early know- search for females. Thus the mating strategies of
ledge of mating behavior by watch ing their moth- the two different male morphs differ conSiderably
ers copulate w ith males. Especially unflanged in the w ay they find potential mates.
males occasionally try to mate with mothers w ith To see whether males have more copulations
small infants; infants almost always respond to with females who are potentially receptive than
these attempts by struggling with the male. with females in a non-reproductive stage (clearly
pregnan t or nursing a dependent infant), we
counted the number of their copulations w ith
16.2.2 Male mating behavior
female s in either stage. Figu re 16.1 shows that, at
Male-male competition has been cited as a major all sites, flanged males copulate more with poten-
determinant of orangutan social organization, tially fertile fema les than with non-fertile females.
in which males compete for access to females Unflanged males show a weaker tendency, but
(Rodman 1973b, 1988; Rijken 1978; Galdikas 1979; more detailed data are needed to detect whether
Mitani 1985a; U tami Atmoko 2000; Utami Atmoko there are real d ifferences between male morphs
et al. in preparation; see Chapter 15). In support of and populations.
this argument, flanged males are highly intoler- A consortship occurs when a male and a female
ant of each other, and their 'long calls' function travel together and show coordination in their
as a spacing mechanism (Mitani 1985a; Mitra behavior for several days or weeks, up to a month,
Setia and van Schaik 2007; see Chapter 15). These during which interactions, including copulations,
same long calls also function as a locator call to may take place (MacKinnon 1974; Rijksen 1978;
females, and attract receptive fema les (Mitra Setia Utami Atmoko 2000). Data from several sites sug-
and van Schall< 2007; see Chapter 17). Receptive gest that adult (parous) females prefer flanged
females may initiate association by approaching a males as consort partners (Galdikas 1979, 1981;
male's long cali, or accept his initiative to associate Mitani 1985b; Rodman and Mitani 1987; Mitra Setia
(Schurmann and van Hooff 1986; see Chapter 17). 1995; Fox 2002). This is confirmed by the available
Unflanged males, on the other hand, cannot attract quantitative data for Ketambe, Sumatra (Fig. 16.2):
females through vocalizations and have to actively almost one half of the copulations by unflanged

Nl64 N353 N55 N15 N42 N24

• ~

100

ID 80
]
.~ 60 o Flanged
~ o Unflanged
-g 40

l
~ 20

o II! 'I 1,1 " 1 111 %.1 I , r I, I I I, I, 0

Ke Su Tu 5, GP Kn
Sumatra Borneo

Figure 16.1 Percentage of copulations by flanged arld unflanged males with reproductive (sexually active) fema les in six different sites.
Numbers above columns indicate total number of copUlations observed and stars indicate significant difference between flanged and
unflanged males in GHj-test: * p <0.05; P <0.01.
U
 240 ORANGUTANS

100
Nt64
m
N353
~.
N43 Nt5 N42
•
N52
~. ...
Nt79

•>
'"e 00
~
§ 60
10o
~
0

-3"0-
.,III I I III I Il J I [I 111
Flanged
Unflanged

..
8 20

0
K, Su I Tu So GP TP Ku
Sumatra Borneo

figure 16.3 Percentage of copulations by both flanged and unflanged males that are cooperative (Le. non-resisted by females) in seven
sites. Numbers above columns indicate total number of copulations observed and stars indicate significant difference between flanged and
unflanged males in G.dj,test: • P <0.05; .. P <0.01; P < 0,Q01 .
I

two of the Bornean sites cooperate in the majority in the proximity of a flanged male. Thus, despite a
of all copulation attempts. In both Sumatran and vulnerability to harassment caused by their semi-
most Bornean sites, except for Gunung Palung, solitary lifestyle, orangutan females not only resist
cooperative matings by females are significantly particular mating attempts, they also can manipu-
more likely with flanged males than with unflanged late mating success of non-preferred males by
males (see Fig. 16.3). However, in most Bornean sites, manoeuvering themselves under the protective
females do resist a higher proportion of mating umbrella of a dominant male. This reasoning also
attempts by flanged males than in Sumatra, sup- implies that the un flanged males are in a 'waiting-
porting the idea that females in both Sumatra and room' situation, making the best of the bad job. In
Borneo have a preference for mating with flanged other words, the unflanged stage is not a perman-
males. However, the differences in female cooper- ent alternative tactic but a transitional stage (Utanti
ation rates for mating with the two male morphs Atmoko and van Hoaff 2004).
are variable and for the Bornean sites based on
small numbers of females. Whether a female resists
16.3 Paternity
a particular mating attempt probably depends not
only on the status and morph of the male, but also So far, only two studies described the genetic con-
on other factors, such as fema le parity and the rela- sequences of the mating strategies of flanged and
tionship between the partners. unflanged males, one in Sumatra (Utami et a/.
Females in association with a non-preferred 2002), and one in Borneo (Goossens et al. 2006b).
male can play an active role in ending the asso- These studies used human-derived microsate1-
ciation, even when they cannot 'outrun' an agile lites to estimate paternity, and showed that both
wUlanged male, who tends to intercept her when unflanged and flanged males are successful in sir-
she flees (e.g. van Schaik 2004). Females can travel ing offspring. In Ketambe, paternity analysis of 11
in the direction of recent long call by dominant offspring born over a 15-year period was carried
males and thus orchestrate a male- male encounter out and 6 out of 10 offspring could be attributed
(Utami and Mitra Setia 1995; Fox 2002). Fox (l998, to 3 un£langed males and 4 to 3 flan ged males in
2002) found in Suaq a dear decrease in mating the area at the time of conception of these offspring
attempts by unflanged males when females stayed (the father for the eleventh offspring could not be
 ORANGUTAN MATING BEHAVIOR AND STRATEGIES 241

Table 16.2 Overview of the database used lor this chapter identified sires for 10 infants born during study period in Ketambe. Infants
(columns) in italics are "om rehabili tant mauilines, others from wild local matrlines. Males (rows) present in year of conception in study area;
names in capitals refer to flanged males, ifllower case to unflanged males. P, present, P', identified as sire.

A", Pot Chris H" Eib Puji y" 'ot G,n K, / Dominant male

Year born 1975 1983 1987 1988 1991 1991 1992 1993 1997 1996
JON P p. P P P P 1972-1990
NUR P P p. p. 1991-1 995
ERIK P A P P P P
MIKI P P P P P
W P P
I P P P Old male?
JAN P 1995 attempt?
BORIS P P 1995-1
DOBA
B08BY p.
A2
Boris p. P P p. p. P P P
B" P P P P P
Wiba P
X p. P P P p.
Dedi P P
Aldo p. P

identified) (see Table 16.2). At least, the available These two latter points may well be related. At
data show that most or all infants were sired dUL- Ketambe, Schurmann (1982) shtdied the socio-
ing voluntary consortships, even if these were not sexual development of an adolescent female. He
with flanged males. noted a slow and very gradual process of develop-
The results from Ketambe suggest roughly equal ing relations between the maturing young female
per capita siring success of unflanged and flanged and males. Young unflanged males were the first
males (Utami et al. 2002), but this conclusion needs to show interest in her and they formed volun-
some qualification. First, six offspring were sired tary consortships with her. The adolescent femal e,
by three (of at least six known) unflanged males. however, showed a clear preference for the bigger,
One of these unflanged males sired three infants flanged males, in particular for the biggest one in
and eventually developed SSCs and became the the area, who in turn only gradually developed an
dominant flanged male in the area. Second, five interest in her. It took a long time, at least 5 years,
of the ten offspring with an identified father were for the adolescent female to build up a relationship,
from matrilines whose founding females were which involved consortship and mating with the
ex-rehabilitants released at Ketambe in the 19705 dominant local flanged male using various kinds
(see Rijksen 1978). Only one of these fi ve was sired of soliciting behavior. It was not until the last year
by a flanged male and none by the then-dominant before she conceived that this dominant local
flanged male in the area. Third, at least four of the flanged male started to react to her elaborate pro-
six offspring sired by unflanged males were born ceptive behavior with 'male presenting'. Flanged
to nulliparous mothers, and only one flanged male males appeared much more interested in older
is known to have sired a first-born offspring of a parous females, who showed less pronounced pro-
wild mother in this sample. ceptive behavior (Schilrmann, 1982). Observations
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